ABSTRACT

Context Pesticides continue to be used on school property, and some schools
are at risk of pesticide drift exposure from neighboring farms, which leads
to pesticide exposure among students and school employees. However, information
on the magnitude of illnesses and risk factors associated with these pesticide
exposures is not available.

Objective To estimate the magnitude of and associated risk factors for pesticide-related
illnesses at schools.

Design, Setting, and Participants Analysis of surveillance data from 1998 to 2002 of 2593 persons with
acute pesticide-related illnesses associated with exposure at schools. Nationwide
information on pesticide-related illnesses is routinely collected by 3 national
pesticide surveillance systems: the National Institute for Occupational Safety
and Health’s Sentinel Event Notification System for Occupational Risks
pesticides program, the California Department of Pesticide Regulation, and
the Toxic Exposure Surveillance System.

Results Incidence rates for 1998-2002 were 7.4 cases per million children and
27.3 cases per million school employee full-time equivalents. The incidence
rates among children increased significantly from 1998 to 2002. Illness of
high severity was found in 3 cases (0.1%), moderate severity in 275 cases
(11%), and low severity in 2315 cases (89%). Most illnesses were associated
with insecticides (n = 895, 35%), disinfectants (n = 830,
32%), repellents (n = 335, 13%), or herbicides (n = 279,
11%). Among 406 cases with detailed information on the source of pesticide
exposure, 281 (69%) were associated with pesticides used at schools and 125
(31%) were associated with pesticide drift exposure from farmland.

Conclusions Pesticide exposure at schools produces acute illnesses among school
employees and students. To prevent pesticide-related illnesses at schools,
implementation of integrated pest management programs in schools, practices
to reduce pesticide drift, and adoption of pesticide spray buffer zones around
schools are recommended.

Exposure to pesticides in the school environment is a health risk facing
children and school employees. Despite efforts of several organizations and
laws in several states to reduce pesticide use at and around schools,1 pesticides continue to be used in schools.2 Another source of pesticide exposure at schools is
from pesticides used on farmland contiguous to school facilities. However,
as a result of the work of the US Environmental Protection Agency (EPA), advocacy
groups, universities, state regulators, the pest control industry, and others,
and laws or strong voluntary programs in several states, pesticide use has
been reduced in some school districts.3

Currently, there are no specific federal requirements on limiting pesticide
exposures at schools. Under the Federal Insecticide, Fungicide, and Rodenticide
Act, pesticides must be registered with the EPA before they are sold or distributed.4 The Food Quality Protection Act5 of
1996 amended the Federal Insecticide, Fungicide, and Rodenticide Act, bolstering
the protection of children through requiring that pesticides used on foods
produce no harm. However, there are no specific provisions in these laws about
the use of pesticides at schools.1,6

The Federal Insecticide, Fungicide, and Rodenticide Act is often supplemented
by more stringent state pesticide laws to protect children from pesticides
at schools. For example, 18 states recommend (n = 6) or require
(n = 12) schools to use integrated pest management strategies and
7 states restrict pesticide applications in areas neighboring a school.7 However, there are still large gaps throughout the
country where children may not be afforded adequate protection.1,8

Pesticide poisoning is a commonly underdiagnosed illness in the United
States today. The clinical findings of acute pesticide poisoning are rarely
pathognomonic but instead can resemble acute upper respiratory tract illness,
conjunctivitis, or gastrointestinal illness, among other conditions. Detailed
description of the diverse syndromes associated with different types of pesticides
is available.9

Although some information about acute illnesses associated with pesticide
exposures at schools is available,10,11 there
has not been an effort to provide a nationwide summary of this health problem.
To estimate the magnitude of and the risk factors for pesticide-related illnesses
associated with exposures at schools, we examined information from state-based
pesticide poisoning surveillance systems (the National Institute for Occupational
Safety and Health’s Sentinel Event Notification System for Occupational
Risks [SENSOR] pesticides program and the California Department of Pesticide
Regulation [CDPR]), and the Toxic Exposure Surveillance System (TESS), which
is a national database of all calls made to poison control centers and is
maintained by the American Association of Poison Control Centers.12,13

METHODS

Study Design and Participants

School employees, parents, and students who developed acute pesticide-related
illnesses from pesticide exposure at child care centers and elementary and
secondary schools from 1998 to 2002 were identified (Table 1). Data were obtained from states participating in the SENSOR
pesticides program (California, Washington, Texas, Florida, Louisiana, New
York, Oregon, and Michigan), CDPR (California), and TESS (all US states and
District of Columbia, with the exception of Hawaii). The data used in these
analyses were surveillance data and as such are exempt from consideration
by the human subjects review board and need for informed consent. Integrating
data from these 3 surveillance systems provides the best available understanding
of the problem of pesticide poisoning at schools. The states participating
in the SENSOR and CDPR programs obtain information from multiple sources (government
agencies, poison control centers, and reports from health care organizations)
and conduct active case follow-up.12 In addition,
all cases identified by the CDPR are referred to the relevant county agricultural
commissioner who investigates the exposure circumstances.10,12 The
TESS data are provided by approximately 67 US poison control centers.13 Approximately 13% of their calls come from physicians
treating patients who are exposed and 87% come from patients or their relatives.12,13

Cases were included if health effects developed subsequent to pesticide
exposure and if these effects were consistent with the known toxicology of
the pesticide product, as determined by state surveillance professionals (SENSOR
and CDPR cases) or a poison control center specialist (TESS cases). The states
participating in the SENSOR pesticides program adopted a standardized case
definition in 1998, and CDPR uses a similar case definition. Briefly, the
case definition required information on pesticide exposure, health effects,
and evidence supporting an association between the pesticide exposure and
the health effects. A full description of the standardized case definition
has been previously published.12 Identification
of TESS cases relied on the experience and judgment of the poison control
center specialist managing the specific case. Multiple cases exposed in a
single exposure incident were identified as 1 exposure event. Exclusion criteria
included exposure to substances other than pesticides, suicides, intentional
abuse, and malicious use.

SENSOR and CDPR primarily capture work-related pesticide poisoning cases,
whereas TESS primarily captures non–work-related cases (Table 1). Detailed information on work-related cases was provided
by SENSOR and CDPR only. The SENSOR and CDPR cases were further classified
into exposure to pesticides applied on school grounds when
indoor and outdoor pesticide applications on school grounds resulted in illness,
and to pesticide drift when pesticide drift from
applications to neighboring farmland resulted in illness among students and
school employees.

For the present analyses, the toxicity category of the pesticide product
was retrieved from a data set made available by the EPA. The EPA assigns acute
toxicity category I to the most toxic pesticide products and category IV to
the least toxic pesticide.14

Illness severity was categorized for SENSOR and CDPR cases using standardized
criteria.15 State agencies classified severity
for the cases they identified in 2001 and 2002. Two authors (W.A.A. and G.M.C.)
assigned severity to 1998-2000 SENSOR cases, all CDPR cases, and all TESS
cases.16 High severity includes cases in which
the illness or injury is severe enough to be considered life-threatening and
commonly involves hospitalization to prevent death. Signs and symptoms include
seizures and pulmonary edema. Moderate severity illness or injury includes
cases of less severe illness or injury often involving systemic manifestations
requiring treatment. The individual is able to return to normal functioning
without any residual disability. Low severity illness or injury typically
resolves without treatment and is often manifested by skin, eye, or upper
respiratory tract irritation.15

Data quality control procedures included the elimination of duplicates
between SENSOR (California) and CDPR, and between SENSOR and CDPR combined
and TESS. To detect duplicates between SENSOR and CDPR combined and TESS,
a case-by-case comparison was performed when a reporting source for SENSOR
and CDPR cases was a poison control center. Cases that matched each other
on state, date of exposure, age, sex, and pesticide name were assumed to involve
the same individual. Such individuals were included only once in the state
agency totals. Six CDPR and 8 TESS duplicates were deleted.

Data Analysis

SAS release 8.02 (SAS Institute Inc, Cary, NC) and Epi Info version
3.2.2 (Centers for Disease Control and Prevention, Atlanta, Ga) were used
for data management and statistical analysis. Age was stratified into children
(<18 years) and adults (≥18 years).

Illness incidence rates among children were calculated. Rate numerators
were obtained by summing the number of ill children reported by year, and
denominators were obtained from the US Census data17 by
summing the number of children in the corresponding state and year. Denominators
were adjusted by subtracting estimates of preschoolers not attending organized
child care centers18 and home-schooled children.19

Illness incidence rates among school employees were calculated for SENSOR
and CDPR cases only. Denominators were obtained from the Current Population
Survey20 by summing the number of full-time
equivalents employed in schools in states and years that contributed to the
numerator. Non–work-related cases (eg, parents) and cases with unknown
work-related status, which included all TESS cases, were not included in these
calculations.

We used odds ratios (ORs) to assess whether age, sex, acute toxicity
pesticide category, surveillance system, or site of pesticide applications
were associated with severity of illness. Odds ratios, 95% confidence intervals
(CIs), χ2 tests, and P values were
calculated using the Epi Info Statcalc utility. SAS release 8.02 was used
to calculate the Poisson regression test for trends in incidence rates across
the years of exposure. P≤.05 was considered statistically
significant.

RESULTS

From 1998 to 2002, 2593 individuals were identified with acute pesticide-related
illnesses associated with pesticide exposures at schools. SENSOR identified
147 cases (6%), CDPR identified 259 cases (10%), and TESS identified 2187
cases (84%) (Table 2). Most illnesses
reported by SENSOR (n = 96, 65%) and CDPR (n = 158, 61%)
were adults, whereas most cases reported by TESS were children (n = 1831,
84%). Among the 2181 persons with known exact age, the mean age for children
was 9.5 years (range, 0.5-17.2 years) and the mean age for adults was 36.1
years (range, 18-76 years).

Information on the toxicity category of pesticides associated with illnesses
was available for 1686 cases (Table 3).
Children were less likely to be exposed to toxicity category I pesticides
compared with adults (14% of children and 42% of adults, P<.001). The odds of high and moderate severity illness were higher
among cases exposed to toxicity category I (18%) than cases exposed to toxicity
category III pesticides (12%) (OR, 1.5; 95% CI, 1.1-2.2). The pesticide active
ingredients associated with high and moderate severity illness are shown in Table 5.

Incidence Rates

The overall incidence rate among children for 1998-2002 was 7.4 cases
per million children (Table 6). The
yearly incidence rates increased from 1998 through 2002 for preschool children
(P<.001), school-aged children (P = .002), and all combined (P<.001).
The overall incidence rate among adults was 27.3 cases per million full-time
equivalents (Table 7), and the yearly
incidence rates decreased from 1998 through 2002 (P<.001).

Table Graphic Jump LocationTable 6. Annual Number and Incidence Rates
per Million of Acute Pesticide-Related Illnesses Among Children, 1998-2002*

Illnesses Reported by SENSOR and CDPR

The SENSOR and CDPR results are combined (Table 2) because the case definition and level of detail are similar.
A total of 406 persons were exposed to pesticides in 173 events for a mean
of 2.3 cases per exposure event (range, 1-61 cases). Eleven exposure events
accounted for 208 cases (51%). The 244 work-related cases were exposed in
155 events.

Occupational Illnesses. Among the 244 work-related
cases, 144 (59%) were not applying pesticides, 93 (38%) were applying or handling
pesticides, and 7 (3%) had no information available. Among the 144 employees
not applying pesticides, 96 (67%) were exposed to pesticides applied on school
grounds and 48 (33%) were exposed to pesticide drift from neighboring farmland.
Sixty-three nonapplicator illnesses (44%) were among teachers. Among the 93
school employees who were applying or handling pesticides, there were 41 custodians
and gardeners, 26 food preparation workers, 7 teachers, 7 maintenance workers,
and 12 unspecified school employees.

Illnesses Associated With Exposure to Pesticides Applied
on School Grounds and Pesticide Drift From Farmland. A total of 281
cases (69%) that were reported to SENSOR and CDPR were exposed to pesticide
applications on school grounds (Table 8).
Insecticides (n = 156, 56%) and disinfectants (n = 99,
35%) accounted for most of the cases. The most common active ingredients were
diazinon (n = 64, 23%), sodium hypochlorite (n = 47, 17%),
chlorpyrifos (n = 40, 14%), quaternary ammonium compound (n = 38,
14%), and malathion (n = 14, 5%).

Table Graphic Jump LocationTable 8. Exposure to Pesticides Applied on
School Grounds vs Pesticide Drift From Farmland in the United States, 1998-2002*

COMMENT

These findings indicate that pesticide exposures at schools continue
to produce acute illnesses among school employees and students in the United
States, albeit mainly of low severity and with relatively low incidence rates.
Illnesses were associated with pesticides applied on school grounds and with
pesticide drift from neighboring farmland. The pesticide exposures at schools
might be associated in part with several factors: a lack of federal and state
regulations regarding pesticide usage in schools1;
regulatory noncompliance by school management, school employees, and pesticide
applicators in states in which regulations and recommendations have been passed;
and insufficient involvement of stakeholders (eg, parents, teachers, students,
school administrators, pest managers).6

We found that the pesticide poisoning incidence rates among children
increased during the period of our report. Given that 40% (n = 59)
of SENSOR and CDPR cases involving children were exposed to pesticide drift
and, given increasing suburban sprawl, this trend among children might be
related to an increased number of schools situated next to farmland.6 Additional studies are needed to confirm this hypothesis.
Hypotheses for the decreasing trend in illness rates among school employees
include changes in pesticide use practices and increased awareness of the
toxic effects of pesticides.

Incidence rates among school employees were found to be higher than
incidence rates among children. Possible explanations include school employees
are called to protect children when incidents occur, whereas students are
often quickly evacuated; school employees are at schools for more hours compared
with students; and some school employees handle or apply pesticides.

Based on SENSOR and CDPR data, most cases of acute pesticide-related
illnesses were associated with pesticides applied on school grounds (n = 281,
69%). Repeated pesticide applications on school grounds raise concerns about
persistent low level exposures to pesticides at schools. It is known that
some pesticides degrade slowly when they are not exposed to sun, rain, and
bacterial action in the soil.21- 24 In
addition, pesticide residues on the school grounds might be tracked into school
buildings by students and school employees. The chronic long-term impacts
of pesticide exposures have not been comprehensively evaluated; therefore,
the potential for chronic health effects from pesticide exposures at schools
should not be dismissed.25 Unfortunately, the
surveillance methods used in our report are inadequate for assessing chronic
effects.

Although insecticides were most frequently associated with pesticide-related
illnesses (n = 895, 35%), we found that exposure to disinfectants
at schools might also be a cause for concern. First, disinfectants accounted
for 830 (32%) of 2593 total cases and for 101 (37%) of 275 moderate severity
cases. Second, 259 (56%) of 461 cases of disinfectant exposure with toxicity
category available were of toxicity category I. Finally, most of the disinfectants
associated with moderate illnesses were products commonly used at schools
(sodium hypochlorite and quaternary ammonium compounds).

We also found acute illnesses associated with exposure to pesticide
drift from neighboring farmland. These exposures might have resulted from
pesticide applicators not complying with pesticide labels, regulations, and/or
guidance to avoid pesticide spray drift, or lack of federal and state regulations
regarding pesticide application around schools. Additionally, pesticide drift
from neighboring farm fields might increase pesticide exposure inside schools.
Some studies26- 29 suggest
that dwellings adjacent to fields can be contaminated by pesticide drift during
applications and subsequent wind recirculation of dust from the fields.

To prevent illnesses associated with pesticide applications on or near
school grounds, there is a need to reduce pesticide use. This can be accomplished
by implementing integrated pest management at schools and using methods that
reduce pesticide drift from farmland. Integrated pest management programs
can reduce pesticide use at schools.3,30 Integrated
pest management is endorsed by the EPA,3 National
Parent Teacher Association,31 National Education
Association, and other organizations. The elements of integrated pest management
are detailed in the Box. Useful
guidance and references on integrated pest management in schools are widely
available.3,32 Some disadvantages
of integrated pest management implementation include the requirements of more
involvement of school employees, parents, and students, and the need to be
educated on pest biology and integrated pest management. Finally, some economic
investment is usually required at the outset of an integrated pest management
program. However, over the long term, the costs of integrated pest management
have been found to be lower than traditional pest control.3,30

Pesticides Applied on School PropertyImplement
school integrated pest management programs:

Monitor for pest problems.

Identify the sources of any pest problems.

Eliminate the sources of any pest problems, using
pesticides only as a last resort. Use nontoxic methods, such as ensuring sanitary
conditions and structural integrity.

If nontoxic pest control methods are impractical
or unsuccessful, then use pesticides having the lowest possible toxicity.
Pesticides in US Environmental Protection Agency toxicity categories I and
II should be avoided if possible. If pesticides are used:

Provide prior written notification of the application.

Post notices in designated areas at the school.

Students and staff should not be present during pesticide applications.

Restrict entry into a previously treated area for a specified duration
following an application.

Call a poison control center or seek medical attention
if pesticide-related illnesses arise.

Trained and qualified workers should handle and apply
pesticides. They must be provided with appropriate safety equipment.

Put the school’s policy on pest control in
writing and distribute it to school stakeholders periodically (eg, at the
beginning of the school year).

Pesticide Drift From Neighboring FarmlandReduce
or eliminate application methods that result in drift.Timing of pesticide
applications. Applications should be performed when students and school employees
are not present.Farmers and pesticide applicators should comply with
labels, regulations, and guidance to avoid pesticide spray drift.Pesticides
should be applied by trained applicators.Establish and enforce nonspray
buffer zones around schools. Size of buffer zone depends on toxicity of pesticide,
type of application (ground or aerial), and weather conditions. For example,
7 states require buffer zones ranging from 300 feet to 2.5 miles around schools.

UnderreportingImprovement in pesticide
poisoning surveillance is needed. Every state should implement an acute pesticide-related
illness surveillance system.Acute pesticide-related illnesses should
be a reportable condition in all states.

We tried to identify illness rate differences among children across
states with different integrated pest management laws (mandatory, voluntary,
without laws). However, this comparison was not meaningful because these laws
have tremendous variation across states in terms of coverage, enforcement,
and implementation. Additionally, 40% of cases among children in SENSOR and
CDPR were exposed to pesticide drift. A similar proportion of children in
the entire data set might have been exposed to pesticide drift but these cases
could not be identified in TESS. Integrated pest management practices in schools
are not designed to prevent exposures to pesticide drift. There were too few
SENSOR and CDPR cases involving onsite applications in schools (n = 281)
to assess integrated pest management laws.

Our findings are subject to at least 3 limitations. First, these results
should be considered low estimates of the magnitude of the problem because
many cases of pesticide poisoning are likely not reported to surveillance
systems or poison control centers. Individuals who do not seek medical care
or report their illness to a surveillance system or a poison control center
will not be identified. Even when individuals seek medical care, their illness
may not be recognized as pesticide-related, because of the nonpathognomonic
nature of the signs and symptoms and because clinicians receive little training
on these illnesses.33,34 Second,
although all of these cases met the definition criteria, the possibility of
some false-positives cannot be excluded. Given both the nonspecificity of
the clinical findings of pesticide poisoning and the lack of a criterion standard
diagnostic test, some illnesses temporally related to pesticide exposures
may be coincidental and not caused by these exposures. Third, although the
case definition was similar, some characteristics of the populations reported
by these 3 systems were different. TESS was efficient in capturing data for
children, but it did not collect information on occupation, work-relatedness,
and the activity the person was performing when exposed to pesticides. The
SENSOR and CDPR data apply to 8 states and principally identify work-related
cases. Not all states participating in SENSOR collect information on nonoccupational
cases; therefore, many cases among children were likely missed by SENSOR and
CDPR. None of these data sources are comprehensive. The literature suggests
that less than one third of poisoning cases treated in health care facilities
are reported to poison control centers and in states where SENSOR and TESS
systems are in place, TESS identified only 10% of the cases identified by
SENSOR.35

In conclusion, despite the limitations of these 3 surveillance systems,
our report is useful in providing national estimates of the magnitude of pesticide-related
illnesses among school employees and students, and in identifying the risk
factors that should be targeted for prevention. Strategies recommended to
reduce pesticide exposures at schools include adopting integrated pest management
programs and using methods to reduce pesticide drift from farmland.

Funding/Support: This study was supported by
the US government through the US Environmental Protection Agency and the Centers
for Disease Control and Prevention, which employs Drs Alarcon, Calvert, and
Blondell.

Role of the Sponsor: The National Institute
for Occupational Safety and Health/Centers for Disease Control and Prevention
(CDC) designed and conducted the study; collected, managed, analyzed, and
interpreted the data; and prepared, reviewed, obtained external peer review,
and approved the manuscript.

Disclaimer: The reviews expressed and the results/conclusions
reached within this article do not necessarily reflect the opinions of the
CDC, US Environmental Protection Agency, or each author’s state agency.

Acknowledgment: We thank Ximena Vergara (Public
Health Institute, Oakland, Calif) who provided support in data management
in the California Department of Health Services; Marty Petersen (National
Institute for Occupational Safety and Health/CDC, Division of Surveillance,
Hazard Evaluation and Field Studies) who provided support in statistical analysis;
Donald Baumgartner (US Environmental Protection Agency, Region V), Sherry
E. Jones (National Center for Chronic Disease Prevention and Health Promotion/CDC,
Division of Adolescent and School Health), and John Palassis (National Institute
for Occupational Safety and Health/CDC, Education and Information Division)
who provided a comprehensive review of this article; and Jia Li (National
Institute for Occupational Safety and Health/CDC, Division of Surveillance,
Hazard Evaluation and Field Studies) who provided information on full-time
equivalents from the US Current Population Survey.

REFERENCES

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June 16, 2005

US National Archives and Records Administration. Code of Federal Regulations: Title 40–Protection of Environment:
Chapter I–Environmental Protection Agency: Part 156–Labeling Requirements
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Centers for Disease Control and Prevention. US National Institute for Occupational Safety and Health. SENSOR–Pesticide
Illness and Injury Surveillance. Available at: http://www.cdc.gov/niosh/topics/pesticides/.
Accessibility verified June 16, 2005

American Association of Poison Control Centers. Toxic Exposure Surveillance System (TESS): Instructions
for the Required Definitions and Fields for TESS 2002.Washington, DC: American Association of Poison Control Centers; 2001:1-131

US Census Bureau. National Population Datasets and Population Estimates
for the US, Regions, and States by Selected Age Groups and Sex. Washington, DC: US Department of Commerce, US Census Bureau; 2003.
Available at: http://www.census.gov/popest/estimates.php. Accessibility
verified June 26, 2005

References

US General Accounting Office. Pesticides: use, effects, and alternatives to pesticides in schools. Washington, DC: US General Accounting Office; 1999. Available at: http://www.gao.gov/archive/2000/rc00017.pdf. Accessibility verified
June 16, 2005

US National Archives and Records Administration. Code of Federal Regulations: Title 40–Protection of Environment:
Chapter I–Environmental Protection Agency: Part 156–Labeling Requirements
for Pesticides and Devices. Available at: http://www.access.gpo.gov/nara/cfr/waisidx_03/40cfr156_03.html. Accessibility verified June 16, 2005

Centers for Disease Control and Prevention. US National Institute for Occupational Safety and Health. SENSOR–Pesticide
Illness and Injury Surveillance. Available at: http://www.cdc.gov/niosh/topics/pesticides/.
Accessibility verified June 16, 2005

American Association of Poison Control Centers. Toxic Exposure Surveillance System (TESS): Instructions
for the Required Definitions and Fields for TESS 2002.Washington, DC: American Association of Poison Control Centers; 2001:1-131

US Census Bureau. National Population Datasets and Population Estimates
for the US, Regions, and States by Selected Age Groups and Sex. Washington, DC: US Department of Commerce, US Census Bureau; 2003.
Available at: http://www.census.gov/popest/estimates.php. Accessibility
verified June 26, 2005

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